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The complete mitochondrial genomes of sixteen ardeid birds revealing the evolutionary process of the gene rearrangements

BACKGROUND: The animal mitochondrial genome is generally considered to be under selection for both compactness and gene order conservation. As more mitochondrial genomes are sequenced, mitochondrial duplications and gene rearrangements have been frequently identified among diverse animal groups. Alt...

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Detalles Bibliográficos
Autores principales: Zhou, Xiaoping, Lin, Qingxian, Fang, Wenzhen, Chen, Xiaolin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4111848/
https://www.ncbi.nlm.nih.gov/pubmed/25001581
http://dx.doi.org/10.1186/1471-2164-15-573
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author Zhou, Xiaoping
Lin, Qingxian
Fang, Wenzhen
Chen, Xiaolin
author_facet Zhou, Xiaoping
Lin, Qingxian
Fang, Wenzhen
Chen, Xiaolin
author_sort Zhou, Xiaoping
collection PubMed
description BACKGROUND: The animal mitochondrial genome is generally considered to be under selection for both compactness and gene order conservation. As more mitochondrial genomes are sequenced, mitochondrial duplications and gene rearrangements have been frequently identified among diverse animal groups. Although several mechanisms of gene rearrangement have been proposed thus far, more observational evidence from major taxa is needed to validate specific mechanisms. In the current study, the complete mitochondrial DNA of sixteen bird species from the family Ardeidae was sequenced and the evolution of mitochondrial gene rearrangements was investigated. The mitochondrial genomes were then used to review the phylogenies of these ardeid birds. RESULTS: The complete mitochondrial genome sequences of the sixteen ardeid birds exhibited four distinct mitochondrial gene orders in which two of them, named as “duplicate tRNA(Glu)–CR” and “duplicate tRNA(Thr)–tRNA(Pro) and CR”, were newly discovered. These gene rearrangements arose from an evolutionary process consistent with the tandem duplication - random loss model (TDRL). Additionally, duplications in these gene orders were near identical in nucleotide sequences within each individual, suggesting that they evolved in concert. Phylogenetic analyses of the sixteen ardeid species supported the idea that Ardea ibis, Ardea modesta and Ardea intermedia should be classified as genus Ardea, and Ixobrychus flavicollis as genus Ixobrychus, and indicated that within the subfamily Ardeinae, Nycticorax nycticorax is closely related to genus Egretta and that Ardeola bacchus and Butorides striatus are closely related to the genus Ardea. CONCLUSIONS: The duplicate tRNAThr–CR gene order is found in most ardeid lineages, suggesting this gene order is the ancestral pattern within these birds and persisted in most lineages via concerted evolution. In two independent lineages, when the concerted evolution stopped in some subsections due to the accumulation of numerous substitutions and deletions, the duplicate tRNAThr–CR gene order was transformed into three other gene orders. The phylogenetic trees produced from concatenated rRNA and protein coding genes have high support values in most nodes, indicating that the mitochondrial genome sequences are promising markers for resolving the phylogenetic issues of ardeid birds when more taxa are added. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-573) contains supplementary material, which is available to authorized users.
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spelling pubmed-41118482014-08-05 The complete mitochondrial genomes of sixteen ardeid birds revealing the evolutionary process of the gene rearrangements Zhou, Xiaoping Lin, Qingxian Fang, Wenzhen Chen, Xiaolin BMC Genomics Research Article BACKGROUND: The animal mitochondrial genome is generally considered to be under selection for both compactness and gene order conservation. As more mitochondrial genomes are sequenced, mitochondrial duplications and gene rearrangements have been frequently identified among diverse animal groups. Although several mechanisms of gene rearrangement have been proposed thus far, more observational evidence from major taxa is needed to validate specific mechanisms. In the current study, the complete mitochondrial DNA of sixteen bird species from the family Ardeidae was sequenced and the evolution of mitochondrial gene rearrangements was investigated. The mitochondrial genomes were then used to review the phylogenies of these ardeid birds. RESULTS: The complete mitochondrial genome sequences of the sixteen ardeid birds exhibited four distinct mitochondrial gene orders in which two of them, named as “duplicate tRNA(Glu)–CR” and “duplicate tRNA(Thr)–tRNA(Pro) and CR”, were newly discovered. These gene rearrangements arose from an evolutionary process consistent with the tandem duplication - random loss model (TDRL). Additionally, duplications in these gene orders were near identical in nucleotide sequences within each individual, suggesting that they evolved in concert. Phylogenetic analyses of the sixteen ardeid species supported the idea that Ardea ibis, Ardea modesta and Ardea intermedia should be classified as genus Ardea, and Ixobrychus flavicollis as genus Ixobrychus, and indicated that within the subfamily Ardeinae, Nycticorax nycticorax is closely related to genus Egretta and that Ardeola bacchus and Butorides striatus are closely related to the genus Ardea. CONCLUSIONS: The duplicate tRNAThr–CR gene order is found in most ardeid lineages, suggesting this gene order is the ancestral pattern within these birds and persisted in most lineages via concerted evolution. In two independent lineages, when the concerted evolution stopped in some subsections due to the accumulation of numerous substitutions and deletions, the duplicate tRNAThr–CR gene order was transformed into three other gene orders. The phylogenetic trees produced from concatenated rRNA and protein coding genes have high support values in most nodes, indicating that the mitochondrial genome sequences are promising markers for resolving the phylogenetic issues of ardeid birds when more taxa are added. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-573) contains supplementary material, which is available to authorized users. BioMed Central 2014-07-08 /pmc/articles/PMC4111848/ /pubmed/25001581 http://dx.doi.org/10.1186/1471-2164-15-573 Text en © Zhou et al.; licensee BioMed Central Ltd. 2014 This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Zhou, Xiaoping
Lin, Qingxian
Fang, Wenzhen
Chen, Xiaolin
The complete mitochondrial genomes of sixteen ardeid birds revealing the evolutionary process of the gene rearrangements
title The complete mitochondrial genomes of sixteen ardeid birds revealing the evolutionary process of the gene rearrangements
title_full The complete mitochondrial genomes of sixteen ardeid birds revealing the evolutionary process of the gene rearrangements
title_fullStr The complete mitochondrial genomes of sixteen ardeid birds revealing the evolutionary process of the gene rearrangements
title_full_unstemmed The complete mitochondrial genomes of sixteen ardeid birds revealing the evolutionary process of the gene rearrangements
title_short The complete mitochondrial genomes of sixteen ardeid birds revealing the evolutionary process of the gene rearrangements
title_sort complete mitochondrial genomes of sixteen ardeid birds revealing the evolutionary process of the gene rearrangements
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4111848/
https://www.ncbi.nlm.nih.gov/pubmed/25001581
http://dx.doi.org/10.1186/1471-2164-15-573
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